Geographic Variation of Diapause and Sensitive Stages of Photoperiodic Response in Laodelphax Striatellus Falle´N (Hemiptera: Delphacidae)

Journal of Insect Science (2016) 16(1): 13; 1–7 doi: 10.1093/jisesa/iev161 Research article

Geographic Variation of Diapause and Sensitive Stages of Photoperiodic Response in Laodelphax striatellus Falle´n (Hemiptera: Delphacidae)

Yang-Yang Hou, Lan-Zhen Xu, Yan Wu, Peng Wang, Jin-Jian Shi, and Bao-Ping Zhai1

Department of Entomology, College of Plant Protection, Nanjing Agricultural University, Nanjing, China ([email protected]; [email protected]; [email protected]; [email protected]; [email protected]) and 1Corresponding author, e-mail: [email protected] Subject Editor: Xinzhi Ni

Received 27 August 2015; Accepted 29 October 2015

Abstract Large numbers of the small brown planthopper Laodelphax striatellus (Falle´ n) (Hemiptera: Delphacidae) occur in temperate regions, causing severe losses in rice, wheat, and other economically important crops. The planthoppers enter diapause in the third- or fourth-instar nymph stage, induced by short photoperiods and low temperatures. To investigate the geographic variation in L. striatellus diapause, we compared the incidence of nymphal diapause under various constant temperature (20 and 27C) and a photoperiod of 4:20, 8:16, 10:14, 12:12, 14:10, and 16:8 (L:D) h regimes among three populations collected from Hanoi (21.02 N, 105.85 E, northern Vietnam), Jiangyan (32.51 N, 120.15 E, eastern China), and Changchun (43.89 N, 125.32 E, north-eastern China). Our results indicated that there were significant geographic variations in the diapause of L. striatellus. When the original latitude of the populations increased, higher diapause incidence and longer critical photoperiod (CP) were exhibited. The CPs of the Jiangyan and Changchun populations were 12 hr 30 min and 13 hr at 20C, and 11 hr and 11 hr 20 min at 27C, respectively. The second- and third-instar nymphs were at the stage most sensitive to the photoperiod. However, when the fourth- and fifth-instar nymphs were transferred to a long photoperiod, the diapause-inducing effect of the short photoperiod on young instars was almost reversed. The considerable geographic variations in the nymphal diapause of L. striatellus reflect their adaptation in response to a variable environment and provide insights to develop effective pest management strategies.

Key words: diapause, geographic variation, Laodelphax striatellus, sensitive stage

Diapause is an important physiological response and an adaptation important to develop new strategies for pest management for insects to survive under adverse environmental or climatic condi- (Denlinger 2008). tions (Tauber et al. 1986; Danks 1987). The diapause characteristics The small brown planthopper Laodelphax striatellus (Falle´n) related to fitness often result from adaptive evolution. Geographic (Hemiptera: Delphacidae) occurs mainly in the temperate zone and variations in diapause are especially interesting for us to study to de- is one of the most destructive agricultural pests (Kisimoto 1958, termine the climatic adaptation of organisms because climate varies 1989). Adults and nymphs suck the sap from a large number of eco- with geography (Danilevsky et al. 1970). Diapause variations nomically important crops, which results in reduced yields and poor among populations have been frequently reported in insects, includ- grain quality (Liu et al. 2006), and the species causes further damage ing hemipterans such as the red firebug, Pyrrhocoris apterus (Socha by transmitting plant viruses (Nault 1994; Nemoto et al. 1994; 2001), Dicyphus hesperus (Gillespie and Quiring 2005), the big- Wang et al. 2014). L. striatellus overwinters as second to fifth-instar eyed bug, Geocoris punctipes (Ruberson et al. 2001), Orius sauteri nymphs in weeds and wheat fields in temperate and cold temperate (Ito and Nakata 2000; Shimizu and Kawasaki 2001; Musolin and zones (Kisimoto 1958, 1989; Cai et al. 1964; Noda 1992; Wang Ito 2008), and Nesidiocoris tenuis (Pazyuk et al. 2014), and these re- et al. 2014). Adults can migrate over a long distance in early summer sults support the hypothesis of local adaptation or adaptation to en- (Sanada-Morimura et al. 2001; Syobu et al. 2011; Wang et al. 2011; vironmental stress. Knowledge of geographic variations in the Zhang et al. 2011; He et al. 2012). diapause of insects clarifies not only the life history traits of insects, The diapause of L. striatellus has been investigated in previous but also their adaptive mechanisms to environments, which is studies. During the development of third- or fourth-instar nymphs,

VC The Author 2016. Published by Oxford University Press on behalf of the Entomological Society of America. 1 This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs licence (http://creativecommons.org/licenses/by- nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work is not altered or transformed in any way, and that the work properly cited. For commercial re-use, please contact [email protected] 2 Journal of Insect Science, 2016, Vol. 16, No. 1

Table 1. Geographic populations of L. striatellus included in the study

Population Location of collection (latitude, longitude, altitude) Climatic condition Mean annual Collection date (abbreviation) temperature (year–month)

HN Hanoi, Vietnam (21.02N, 105.85E, 10 m) Tropical zone 21C 2011 April JY Jiangyan, Jiangsu Province, China (32.51 N, 120.15E, 3 m) Subtropical zone 14.6C 2011 May CC Changchun, Jilin Province, China (43.89N, 125.32E, 236 m) Temperate zone 5.2C 2011 July

Data of mean annual temperature (from 1979 to 2012) were obtained from China Meteorological Data Sharing Service System (http://cdc.cma.gov.cn/). the planthoppers might enter diapause that is induced by short pho- tube were renewed every 2 d to avoid wilting of the rice. toperiods at low temperatures. The photoperiodic response curves Molting was checked daily to confirm the nymphal instar; 53–108 indicated a typical long-day response type (Kisimoto 1958, 1989; individuals were included in each of three replicates for all Noda 1992; Wang et al. 2014). As temperature decreases, L. stria- treatments. tellus shows a higher diapause incidence with a longer critical pho- All of the experiments were conducted in illuminated incubators toperiod (CP: the photoperiod in which 50% of individuals enter with four 30-W fluorescent tubes controlled by an automatic time diapause). However, short photoperiods hardly induce diapause at switch (Bic-300, Shanghai Boxun Industry & Commerce Co., Ltd, all at high temperatures (Noda 1992; Wang et al. 2014). In Medical Equipment Factory, Shanghai, China). The light intensity Nanchang, e.g., the induction of photoperiodic diapauses is nearly was held between 500 and 600 lx, and the temperature variation completely inhibited at temperatures under 28C(Wang et al. was 60.5C. 2014). Meanwhile, a long photoperiod or high temperature acted as a diapause-terminating stimulus for L. striatellus nymphs (Noda Criterion for Diapause 1992; Wang et al. 2014), and 26–28 C has been found to be the The diapause of a nymph was defined as its failure to grow into an optimal temperature for diapause termination (Wang et al. 2014). adult at a specific age, which was considered as the maximum time L. striatellus is widely distributed in temperate, tropical, and taken for the development from egg to adult under a diapause-sup- subtropical zones, although it is rampant mainly in the temperate pressing photoperiodic regime (Vinogradova 1974; Rock et al. zone (Kisimoto 1989). Therefore, it is critical to uncover the char- 1983; Rock and Shaffer 1983). This age varies with temperature acteristics of diapause in different geographic populations. and population. As the nymphal diapause of L. striatellus is induced Geographic variation in the diapause of L. striatellus has, so far, by short photoperiods, long photoperiods would serve as a dia- only been reported by Noda (1992), who identified significant dif- pause-suppressing photoperiodic regime for this planthopper. In this ferences in the diapause patterns of nine local populations in study, we set up two long photoperiods of 16:8 and 14:10 (L:D) h, Japan. However, in other important rice-planting regions including and preliminary experiments provided evidence that the nymphs China and Southeast Asian areas, geographic variations have not developed more quickly under a long photoperiod of 16:8 (L:D) h been fully understood. than under 14:10 (L:D) h. Therefore, to more precisely identify the In this study, we compared the diapause characteristics of three diapause of individuals from each of the three populations, we com- L. striatellus populations collected from three regions of Vietnam pared the average development time under the two long photoper- and China by measuring diapause incidence under various constant iods at 20 and 27C, respectively. If the differences were significant, temperature and photoperiod regimes, aiming to reveal the geo- the age was determined as the maximum development time (MDT) graphical variations in diapause in this insect. of nymphs under 16:8 (L:D) h; otherwise, the age was the MDT of nymphs under the two long photoperiods. Materials and Methods Determination of the Sensitive Stage to Diapause Induction Insect To determine the sensitive stage to diapause induction, experiments Three populations of L. striatellus were collected from Hanoi, were performed for the JY and CCs following the method described Vietnam, in the tropical zone (21.02 N, 105.85 E, called ‘Hanoi by Eizaguirre et al. (1994) and Spieth (1995). The HN was excluded population, HN’); Jiangyan, Jiangsu Province, China, in the sub- here because its diapause response to photoperiods was very weak. tropical zone (32.51 N, 120.15 E, called ‘Jiangyan population, Nymphs from the Changchun and JYs were transferred from long JY’); and Changchun, Jilin Province, China, in the temperate zone photoperiod of (16:8) h to short photoperiod of (10:14) h or vice (43.89 N, 125.32 E, called ‘Changchun population, CC’) for this versa at various nymphal stages at 20C. Two photoperiods of 16:8 study (Table 1). The insects were reared on rice in the laboratory at and 10:14 (L:D) h were selected to detect the sensitive stage of 25C with a long photoperiod of 16:8 (L:D) h for one generation L. striatellus, because none of the nymphs entered diapause under before use. the long photoperiod of 16:8 (L:D) h, while most nymphs entered diapause under the short photoperiod of 10:14 (L:D) h at 20C. The Effect of Photoperiod and Temperature on Nymphal Development development time and diapause incidence of these nymphs under the One-day-old male and female adults were paired in a 500-ml treated conditions were examined; 57–102 individuals were transparent cup with rice seedlings for feeding and oviposition. included in each of three replicates for all treatments. The cups were transferred to six photoperiodic conditions of 4:20, 8:16, 10:14, 12:12, 14:10, and 16:8 (L:D) h at both 20 and 27C, Statistical Analysis respectively. Each nymph hatching within 12 hr was reared in The development times of nymphs under the two long photoperiods a glass test tube (1.5 cm in diameter and 20 cm in length) with a of 16:8 and 14:10 (L:D) h were compared using a Student’s t-test. fresh rice seedling until eclosion. The seedling and the glass The diapause incidences were statistically examined using Tukey’s Journal of Insect Science, 2016, Vol. 16, No. 1 3

Table 2. Nymphal average and MDT of L. striatellus in the three geographic populations under 2 long-day photoperiods at 20 and 27C

Temperature Population Development time (d)

Average Maximum

Day length—14hr Day length—16 hr Day length—14 hr Day length—16 hr

20C HY 31.52 6 0.44 32.20 6 0.40 47 45 JY 38.02 6 0.63 37.78 6 0.43 49 47 CC 48.46 6 1.99a 43.53 6 0.79 80 72 27C HY 14.49 6 0.20 13.98 6 0.37 21 18 JY 16.51 6 0.40 16.28 6 0.54 28 27 CC 22.45 6 0.69 21.51 6 0.67 32 30

Data of average development time in the table are means 6 SE. aThe signiﬁcant difference of average development time between 2 long-day photoperiods of 14:10 and 16:8 (L:D) h within the same population at the same temperature in by Student’s t-test (P < 0.05). The sample size for each treatment varied from 268 to 315. HN, Hanoi population; JY, Jiangyan population; CC, Changchun population. honestly significant difference (HSD) test with arcsin square-root transformation. Logistic regression analysis (Sokal and Rohlf 1995) was conducted to decide whether the photoperiod, temperature, and population significantly affected the incidence of diapause. In this study, the dependent variables were assumed as 0 and 1 in the cases of non-diapause and diapause, respectively. All statistical analyses were conducted using the SAS statistical program (SAS Institute Inc. 2002).

Results Criterion for Diapause No significant differences were observed for the average development time between the two long photoperiods of 14:10 and 16:8 (L:D) h at both 20 and 27C for the Hanoi and JYs as well as for the CC at 27C (Student’s t-test: HN, 20C, P ¼ 0.207; 27C, P ¼ 0.0786; JY, 20C, P ¼ 0.1415; 27C, P ¼ 0.7320; CC, 27C, P ¼ 0.1455; Table 2). For the CC, however, a significant difference was observed between the development times under 14:10 and 16:8 (L:D) h at 20C (CC, 20C, P < 0.0001). Therefore, the criterion for diapause in nymphs of the Hanoi and JYs was the MDT under the two long photoperiods. For the CC, at 27C, the criterion was also the MDT at each photoperiod and, at 20C, it was the MDT under a photoperiod of 6:8 (L:D) h. As shown in the results, at 20C, the nymphs not growing into adults after 47, 49, and 72 d from birth were considered diapause for the Hanoi, Jiangyan, and CCs, respectively; at 27C, the diapause criteria were 21, 28, and 32 d, respectively.

Geographic Variation in Diapause Induction Fig. 1. Photoperiodic response curves for nymphal diapause induction in The typical long photoperiodic response was found in all three pop- L. striatellus for three populations at 20C (A) and 27C (B). The CPs were ulations at 20 and 27C, except for the HN at 27C(Fig. 1). 12 hr 30 min (CP1) at 20C and 11 hr (CP3) at 27C in the JY, and 13 hr (CP2) Significant differences in diapause incidence were observed among at 20 C and 11 hr 20 min (CP4) at 27 C in the CC. Different uppercase letters indicate signiﬁcant differences in the diapause incidences among the three the three populations under the same diapause-inducing photoper- populations at the same photoperiod and temperature. Diapause incidences iod [Tukey’s HSD test: 20 C, 4:20 (L:D) h, df ¼ 2, 6, F ¼ 165.99, were arcsin square-root transformed prior to analysis. The sample size for P < 0.0001; 8:16 (L:D) h, df ¼ 2, 6, F ¼ 68.74, P < 0.0001; 10:14 each treatment varied from 174 to 315. HN, Hanoi population; JY, Jiangyan (L:D) h, df ¼ 2, 6, F ¼ 63.04, P < 0.0001; 12:12 (L:D) h, df ¼ 2, 6, population; CC, Changchun population. F ¼ 56.37, P < 0.0001; 27C, 4:20 (L:D) h, df ¼ 2, 6, F ¼ 1.00, P ¼ 0.42; 8:16 (L:D) h, df ¼ 2, 6, F ¼ 14.78, P ¼ 0.0048; 10:14 (L:D) of 14:10 (L:D) h, a small number of nymphs entered diapause. The h, df ¼ 2, 6, F ¼ 72.75, P < 0.0001; 12:12 (L:D) h, df ¼ 2, 6, diapause incidence of the JY was lower than that of the CC under F ¼ 4.91, P ¼ 0.0055; Fig. 1]. The most northern population the same conditions, which was only 33.14% at 20C under the (Changchun) exhibited the highest diapause incidence; it is worth photoperiod of 4:20 (L:D) h. The HN had a very weak response to noting that the diapause incidence reached nearly 100% at 20C photoperiods, with fewer than 50% of the individuals entering dia- when the day length was 12 hr. Even under the long photoperiod pause under all photoperiods, and they even displayed no 4 Journal of Insect Science, 2016, Vol. 16, No. 1 photoperiodic response at 27C. Also, as the temperature increased were then transferred to the short photoperiod mimicked the natural to 27C, the diapause incidences decreased in each population. light conditions in late autumn. In these experiments, only a few Logistic regression analysis indicated that the photoperiod, tempera- nymphs entered diapause when they were transferred to the dia- ture, population origin, and the interactions of these factors signifi- pause-inducing photoperiod of 10:14 (L:D) h after completing their cantly affect the incidence of diapause (Table 3). second instar under a diapause-suppressing photoperiod of 16:8 The CP became longer as the latitude increased and the tempera- (L:D) h (JY and CC: diapause incidence <20%; Fig. 2; treatments B, ture decreased (Fig. 1). The results showed that the CPs were 13 hr C, and D). However, >70% of the nymphs entered diapause when at 20C and 11 hr 20 min at 27C in the northern-most population they were transferred to the diapause-inducing photoperiod of 10:14 (Changchun). For the more southern population (Jiangyan), the CPs (L:D) h in the second instar (JY: 73.34%; CC: 88.00%; Fig. 2; treat- were 12 hr 30 min at 20C and 11 hr at 27C. The CP of the HN ment E). Therefore, the second instar was considered to be the most cannot be estimated in this. sensitive to the photoperiod. Furthermore, there were high diapause incidences when the nymphs were constantly exposed to the short photoperiod of 10:14 (L:D) h (JY: 89.63%; CC: 94.70%; Fig. 2, Determination of the Sensitive Stage to Diapause Induction treatment F). The diapause incidences remained high when the The results showed that the diapause incidences were significantly nymphs reared under the long photoperiod only in the fourth instars different among the nymphs that experienced a short photoperiod at (JY: 61.62%; CC: 69.28%; Fig. 2, treatment L). However, when the different ages (Tukey’s HSD test: JY, df ¼ 13, 28, F ¼ 109.32, diapause-inducing photoperiod of 10:14 (L:D) h was interrupted P < 0.0001; CC, df ¼ 13, 28, F ¼ 203.49, P < 0.0001; Fig. 2). The by a long photoperiod of 16:8 (L:D) h only in the third instar, the experiments in which the nymphs reared under the long photoperiod diapause incidences decreased sharply (JY: 24.77%; CC: 32.33%; Fig. 2, treatment K). Thus, the third instar was also a photoperiodically sensitive stage in the JY and CCs. Table 3. Logistic regression results indicating the effects of photo- When the nymphs reared under the short photoperiod were trans- period, population and temperature on diapause induction of L. striatellus ferred to the long photoperiod, the incidence of diapause exceeded 50% only when the nymphs experienced the short photoperiod from Effect DF v2 P the first to the fourth instar (JY: 83.37%; CC: 94.30%; Fig. 2, treatment G). There were low diapause incidences when nymphs were Photoperiod 1 67.18 <0.0001 Population 2 116.75 <0.0001 transferred from the short to the long photoperiod in the fourth-instar Temperature 1 94.11 <0.0001 stage (JY: 37.57%; CC: 46.57%; Fig. 2; treatment H), and low inci- Photoperiod * Population 2 25.77 <0.0001 dences of diapause also occurred when only the third- or fourth-instar Photoperiod * Temperature 1 34.55 <0.0001 nymphs were under the short photoperiod (the third instar: JY, 0%; Population * Temperature 2 47.72 <0.0001 CC,0%;thefourthinstar:JY,10.75%;CC,13.32%;Fig. 2, treat- Photoperiod * Population * Temperature 2 31.52 <0.0001 ments M and N). The results suggest that the diapause incidence of nymphs also depended on the duration of the short photoperiod that

Fig. 2. The nymphal diapause incidences in populations of Jiangyan and Changchun that were transferred from the short photoperiod of 10:14 (L:D) h to the long photoperiod of 16:8(L:D) h vice versa at various nymphal stages. Diapause incidences in figure are means 6 SE. Means followed by different lowercase letters within the same column are significantly different by Tukey’s HSD test (P < 0.05) among different treatments. Diapause incidences were arcsin square-root transformed prior to analysis. The sample size for each treatment varied from 163 to 226. White bars represent the long photoperiod of 16:8 (L:D) h and black bars represent the short photoperiod of 10:14 (L:D) h. JY, Jiangyan population; CC, Changchun population. Journal of Insect Science, 2016, Vol. 16, No. 1 5 the nymph experienced, although the sensitive stages of the Jiangyan Suwa and Gotoh 2006; Timer et al. 2010; Wang et al. 2012). and CCs are the second and third instars. However, in China, the CPs for diapause induction in the Nanchang, Jiangyan, and CCs of L. striatellus only varied by about 1 hr under a range of 14 degrees of latitude. The possible factor underlying the difference in CPs with latitudinal variation between Discussion China and Japan was analyzed as follows. Several reports have The photoperiod is a reliable indicator that can be used to predict proved that extensive gene flow can reduce the genetic variation in unfavorable conditions for insects. Temperature is a less dependable diapause characteristics of different populations (Danilevsky et al. factor but it can modify the photoperiodic response in several insects 1970; Mcwatters and Saunders 1996; Suwa and Gotoh 2006), and (Saunders 1982; Hodkova and Socha 1995; Christiansen-Weniger even lead to a lack of clinal variation in CP (Kimura et al. 1993). In and Hardie 1999). In this study, the results clearly showed that both Japan, significant differentiation among the genetic structure of the photoperiod and the temperature can significantly affect dia- populations of L. striatellus was revealed based on three allozyme pause in L. striatellus, although the diapause incidence and intensity loci, which suggests that long-range dispersal of L. striatellus does varied among populations (Fig. 1, Table 3). Our results were consis- not regularly occur over the main lands (Hoshizaki 1997). tent with those of Kisimoto (1958), Noda (1992), and Wang et al. Moreover, although the overseas migration of L. striatellus from (2014), but these studies showed that the diapause incidence was the East China Sea and south-eastern Asia to western Japan occurs 100% under the photoperiod of 10:14 (L:D) h. We found that only (Otuka et al. 2010; Sanada-Morimura 2001; Syobu et al. 2011), the CC had a high diapause incidence (nearly 100%) at 20C, and the offspring of the immigrants have low adaptability to the local the Jaingyan and HNs had lower incidences. Therefore, the diapause climate conditions at the landing site (Hoshizaki 1997). From the traits are different among geographic populations of L. striatellus. earlier studies, we infer that gene flow among the L. striatellus pop- Variation in photoperiod-inducing diapause along with latitude ulations in Japan is low. In China, however, L. striatellus can is well known in many insect species. Generally, there are higher dia- undertake long-distance migration and intercross between domes- pause incidences and longer CPs in northern populations than in tic populations, suggesting extensive gene flow (Wang et al. 2011; southern ones (Danilevskii 1965; Danilevsky et al. 1970; Tauber Zhang et al. 2011; He et al. 2012; Sun et al. 2015). As a result, and Tauber 1972; Beck 1980; Wang et al. 2012), and this phenom- L. striatellus populations lack significant genetic differences in enon was also found in L. striatellus in this study. The most north- China (Sun et al. 2015). Therefore, we infer that the different ern population (Changchun) showed the highest diapause incidence degrees of variation in diapause with latitude between Japan and and a longer CP, where even some nymphs entered diapause under China are due to the different levels of gene flow among the domes- the long photoperiod of 14:10 (L:D) h. However, the most southern tic populations in the two countries. population (Hanoi) showed the lowest diapause incidence and dis- Our results indicated that the sensitive stage to photoperiods in played no photoperiodic response at 27C. Noda (1992) reported the Jiangyan and CCs was the third instar, which was consistent that a similar phenomenon also emerged in the diapause pattern of with that of the Nanchang population as reported by Wang et al. nine local populations in Japan. Northern populations overwinter (2014). Additionally, the results in the experiment of transferring for a longer period than southern ones, so greater diapause intensity nymphs from the long day length of 16:8 (L:D) h to the short day is required by populations in northern areas. Additionally, relative length of 10:14 (L:D) h proved that the second instar was also a to southern areas, winter arrives earlier in northern areas and is photoperiodically sensitive stage in the two populations. Like accompanied by longer day lengths, so northern L. striatellus popu- many other insect species, the sensitive stage of L. striatellus tends lations have a longer CP (Danilevsky et al. 1970; Tauber et al. 1986; to be the age immediately preceding the diapause stage (Danks Umsalama et al. 2007; Bradshaw and Holzapfel 2010; Wang et al. 1987), offering obvious advantages of preparation for the upcom- 2012). The annual minimum temperature experienced by the most ing winter and conferring better adaptation to overwintering in southern population (Hanoi) in this study is 13C (data set for the field. However, although the second and third instars were the 1979–2012; China Meteorological Data Sharing Service System, sensitive stages to the photoperiod in L. striatellus, the diapause 2015: http://cdc.cma.gov.cn/), which is close to the threshold tem- incidences depended on the duration of the short photoperiod that perature for the development of L. striatellus (15C) (Zhang et al. the nymph experienced. We conferred that these phenomena 2008). As a result, diapause is not a necessary trait in the HN for would result from two factors. The first is that L. striatellus,like overwinter. Thus, based on the earlier studies, we infer that such many other insects (Danks 1987), could terminate diapause under variability in diapause among L. striatellus populations can be long day lengths (Noda 1992; Wang et al. 2014). The second is attributed to an adaptation to each of the local environmental that the fourth- and fifth-instar periods were also under the con- conditions. trol of photoperiodism in addition to the young instars (Kisimoto Wang et al. (2014) found that the CP of the L. striatellus popu- 1958). Thus, when the nymphs were transferred to a long photo- lation in Nanchang, China (28.8 N, 115.90 E) was 12 hr at 20C period during the later nymphal stages, the diapause-inducing and, here, the CPs of the Jiangyan (32.51 N, 120.15 E) and effect of a short photoperiod on young instars was almost Changchun (43.89 N, 125.32 E) populations were 12 hr 30 min reversed. and 13 hr at 20C, respectively. An obvious gradual clinal type Entering diapause actually confers costs as well as benefits. with latitudinal variation in the CP of L. striatellus was found. A During the period of diapause, the individuals might miss chances similar diapause pattern with latitudinal variation was also found to reproduce and will consume energy reserves, or be killed by in Japan by Noda (1992). Specifically, the CPs of nine populations predators or parasitic animals. Under these circumstances, a risk- in Japan were positively correlated with the original latitude and spreading strategy, which is expressed as the existence of both dia- gradually decreased toward the south at a rate of about 1.1 hr for pausing and non-diapausing individuals under short photoperiod each 5 degrees of latitude, which was in accordance with the rela- here, may be selected (Kurota and Shimada 2001; Caceres and tionship found in many long-day species (Danilevsky et al. 1970; Tessier 2004a,b; Umsalama et al. 2007). In our experiments, the Beck 1980; Tauber et al. 1986; Danks 1987; Ito and Nakata 2000; response of diapause induction to photoperiods is not an ‘all-or- 6 Journal of Insect Science, 2016, Vol. 16, No. 1 nothing’ reaction; no treatment under short day lengths resulted in Ito, K. and T. Nakata. 2000. Geographical variation of photoperiodic reponse a 100% diapause incidence. We infer that, in the field, when the in the females of a predatory bug, Orius sauteri (Poppius) (Heteroptera: CP occurs with a shortened day length, some nymphs will grow Anthocoridae) from northern Japan. Appl. Entomol. Zool. 35: 101–105. slowly and enter diapause. However, other nymphs will grow con- Kisimoto, R. 1958. Studies on the diapause in the planthoppers, effect of photoperiod on the induction and the completion of diapause in the fourth lar- tinuously to adulthood, and these adults will migrate, disperse, val stage of the small brown planthopper, Delphacodes striatella Falleń. and reproduce. This is a risk-spreading strategy formed during Japanese J. Appl. Entomol. Zool. 2: 128–134. long-term evolution to ensure the survival of L. striatellus Kisimoto, R. 1989. Flexible diapause response to photoperiod of a laboratory populations. selected line in the small brown planthopper, Laodelphax striatellus Falleń. In conclusion, although L. striatellus migrates over long distan- Appl. Entomol. Zool. 24: 157–159. ces, populations maintain their particular diapause characteristics to Kimura, M. T., A. Bessho, and Z. H. Dai. 1993. The influence of gene flow on adapt to the local environment. This conservatism appears condu- latitudinal clines of photoperiodic adult diapause in the Drosophila auraria cive to advantageous selections in planthoppers, through which they species-complex. Biol. J. Linn. Soc. 48: 335–341. have adapted to survive the cold winters. Our results provide impor- Kurota, H., and M. Shimada. 2001. Photoperiod- and temperature-dependent tant insights into one possible mechanism underlying adaptation of induction of larval diapause in a multivoltine bruchid, Bruchidius dorsalis. Entomol. Exp. Appl. 99: 361–369. pests to the complicated and volatile climate conditions. Liu, X. D., B. P. Zhai, and C. M. Liu. 2006. Outbreak reasons of Laodelphax Understanding the geographic variation in diapause characteristics striatellus population. Chinese B. Entomol. 43: 141–146 (in Chinese with of L. striatellus may be useful for improving strategies to pest man- English summary). agement, according to which the outbreak of L. striatellus can be Mcwatters, H. G., and D. S. Saunders. 1996. The influence of each parent and predicted more precisely. geographic origin on larval diapause in the blow fly, Calliphora vicina. J. Insect physio. 42: 721–726. Musolin, D. L., and K. T. Ito. 2008. Photoperiodic and temperature control of Acknowledgments nymphal development and induction of reproductive diapause in two predatory Orius bug: interspecific and geographic differences. Physiol. Entomol. This study was supported by a grant from the National Basic Research 33: 291–301. Program of China Program (2010CB126200) and the Special Research Fund Nault, L. R. 1994. Transmission biology, vector specificity and evolution of for the Doctoral Program of Higher Education (20120097110037). planthopper-transmitted plant viruses, pp. 429–448. In R. E. Denno and T. J. Perfect (eds.), Planthopper, their ecology and management. Chapman & References Cited Hall, New York. Nemoto, H., K. Ishikawa, and E. Shimura. 1994. The resistances to rice stripe Beck, S. D. 1980. Insect photoperiodism. 2nd ed. Academic Press, Inc., New York. virus and small brown planthopper in rice variety, IR 50. Breeding Sci. 44: Bradshaw, W. E., and C. M. Holzapfel. 2010. Light, time, and the physiology 13–18. of biotic response to rapid climate change in animals. Annu. Rev. Physiol. Noda, H. 1992. Geographic-variation of nymphal diapause in the small brown 72: 147–166. planthopper in Japan. Japan Agr. Res. Q. 26: 124–129. Cai, B. H., F. S. Huang, W. X. Feng, Y. R. Fu, and Q. F. Dong. 1964. Study on Otuka, A., M. Matsumura, S. Sanada-Morimura, H. Takeuchi, T. Watanabe, Delphacodes striatellus Falleń (Hemiptera: Delphacidae) in North China. R. Ohstu, and H. Inoue. 2010. The 2008 overseas mass migration of Acta Entomol. Sinica 13: 552–571 (in Chinese). the small brown planthopper, Laodelphax striatellus, and subsequent Caceres, C. E., and A. J. Tessier. 2004a. Incidence of diapause varies among outbreak of rice stripe disease in western Japan. Appl. Entomol. Zool. 45: populations of Daphnia pulicaria. Oecologia 141: 425–431. 259–266. Caceres, C. E., and A. J. Tessier. 2004b. To sink or swim: variable diapause Pazyuk, I. M. D. L. .Musolin S. Y. Reznik. 2014. Geographic variation in ther- strategies among Daphnia species. Limnol. Oceanogr. 49: 1333–1340. mal and photoperiodic effects on development of zoophytophagous plant Christiansen-Weniger, P., and J. Hardie. 1999. Environmental and physiologi- bug Nesidiocoris tenuis. J. Appl. Entomol. 138: 36–44. cal factors for diapause induction and termination in the aphid parasitoid, Rock, G. C., P. L. Shaffer, and A. D. Shaltout. 1983. Tufted apple budmoth Aphidius ervi (Hymenoptera: Aphidiidae). J. Insect Physiol. 45: 357–364. (Lepidoptera: Tortricidae): photoperiodic induction of larval diapause and Danilevskii, A. S. 1965. Photoperiodism and seasonal development of insects. stages sensitive to induction. Environ. Entomol. 12: 69–70. Oliver and Boyd, Edinburgh. Rock, G. C., and P. L. Shaffer. 1983. Tufted apple budmoth (Lepidoptera: Danilevsky, A. S., N. I. Goryshin, and V. P. Tyschenko. 1970. Biological Tortricidae): Effects of constant daylengths and temperatures on larval dia- rhythms in terrestrial arthropods. Annu. Rev. Entomol. 15: 201–244. pause. Environ. Entomol. 12: 71–75. Danks, H.V. 1987. Insect dormancy: an ecological perspective. Biological Ruberson, J. R., K. V. Yeargan, and B. L. Newton. 2001. Variation in Survey of Canada, Ottawa, Canada. diapause responses between geographic populations of the predator Denlinger, D.L. 2008. Why study diapause. Entomol. Res. 38: 1–9. Geocoris punctipes (Heteroptera: Geocoridae). Ann. Entomol. Soc. Am. 94: Eizaguirre, M., C. LO´ pez, L. AsIń, and R. Albajes. 1994. Thermoperiodism, 116–122. photoperiodism and sensitive stage in the diapause induction of Sesamia Sanada-Morimura, S., S. Sakumoto, R. Ohtsu, A. Otuka, S. Huang, D. V. nonagrioides (Lepidoptera: Noctuidae). J. Insect Physiol. 40: 113–119. Thanh, and M. Matsumura. 2001. Current status of insecticide resistance in Gillespie, D. R., and D.M.J. Quiring. 2005. Diapause induction under green- the small brown planthopper, Laodelphax striatellus, in Japan, Taiwan, and house condition in two populations of Dicyphus hesperus (Hemiptera: Vietnam. Appl. Entomol. Zool. 46: 65–73. Miridae). Biocontrol Sci. Techn. 15: 571–583. Saunders, D. S. 1982. Insect clocks. Pergamon, Oxford. He, Y., Y. B. Zhu, Y. Y. Hou, S. T. Yao, Z. J. Lu, Z. H. Jin, X. X. Zhang, and B. Shimizu, T., and K. Kawasaki. 2001. Geographic variability in diapause re- P. Zhai. 2012. Fluctuation and migration of spring population of small brown sponse of Japanese Orius species. Entomol. Exp. Appl. 98: 303–316. planthopper (Laodelphax striatellus) on wheat in Jiangsu and Zhejiang prov- Socha, R. 2001. Latitudinal gradient in response of wing polymorphism to inces. Chinese J. Rice Sci. 26: 109–117 (in Chinese with English summary). photoperiod in a flightless bug, Pyrrhocoris apterus (Heteropera: Hodkova, M., and R. Shoca. 1995. Effect of temperature on photoperiodic re- Pyrrhocoris). Eur. J. Entomol. 98: 167–169. sponse in a selected ‘non-diapause’ strain of Pyrrhocoris apterus Sokal, R. R., and F. J. Rohlf. 1995. Biometry: the principles and practice of (Heteroptera). Physiol. Entomol. 20: 303–308. statistics in biological research, 3rd ed. W. H. Freeman & Company, New Hoshizaki, S. 1997. Allozyme polymorphism and geographic variation in the York. small brown planthopper, Laodelphax striatellus (Homoptera: Spieth, H. R. 1995. Change in photoperiodic sensitivity during larval develop- Delphacidae). Biochem. Genet. 35: 383–393. ment of Pieris brassicae. J. Inscet Physiol. 41: 77–83. Journal of Insect Science, 2016, Vol. 16, No. 1 7

Suwa, A., and T. Gotoh. 2006. Geographic variation in diapause induction Vinogradova, E. B. 1974. The pattern of reactivation of diapausing larvae in and mode of diapause inheritance in Tetranychus pueraricola. J. Appl. the blowfly, Calliphora vicina. J. Insect Physiol. 20: 2487–2496. Entomol. 130: 329–335. Wang, L., C. Hang, Y. B. Xu, G. C. Cai, Y. W. Sun, X. Y. Hu, X. X. Zhang, Syobu, S., A. Otuka, and M. Matsumura. 2011. Trap catches of the small and B. P. Zhai. 2011. Migration and dispersal of the small brown planthop- brown planthopper, Laodelphax striatellus (Falleń) (Hemiptera: per Laodelphax striatellus (Falleń) in the Jianghuai region: Case studies in Delphacidae), in northern Kyushu district, Japan in relation to weather con- Fengtai, Anhui Province in spring of 2009 and 2010. Chinese J. Appl. ditions. Appl. Entomol. Zool. 46: 41–50. Entomol. 48: 1288–1297 (in Chinese with English summary). Sun, J. T., M. M. Wang, Y. K. Zhang, M. P. Chapuis, X. Y. Jiang, G. Hu, X. Wang, L. F., K. J. Lin, C. Chen, S. Fu, and F. S. Xue. 2014. Diapause induction M. Yang, C. Ge, X. F. Xue, and X. Y. Hong. 2015. Evidence for high dis- and termination in the small brown planthopper, Laodelphax striatellus persal ability and mito-nuclear discordance in the small brown planthopper, (Hemiptera: Delphacidae). PLoS One, 9, e107030. Laodelphax striatellus. Sci Rep-UK. 5: 8045. Wang, X. P., Q. S. Yang, P. Dalin, X. M. Zhou, Z. W. Luo, and C. L. Lei. Tauber, M. J., and C. A. Tauber. 1972. Geographic variation in critical photo- 2012. Geographic variation in photoperiodic diapause induction and dia- period and in diapause intensity of chrysopa carnea (Neuroptera). J. Inscet pause intensity in Sericinus montelus (Lepidoptera: Papilionidae). Insect Sci. Physiol. 18: 25–29. 19: 295–302. Tauber, M. J., C. A. Tauber, and S. Masaki. 1986. Seasonal adaptations of in- Zhang, A. M., X. D. Liu, B. P. Zhai, and X. Y. Gu. 2008. Influences of temper- sects. Oxford University Press, New York. ature on biological characteristics of the small brown planthopper, Timer, J., P. C. Tobin, and M. C. Saunders. 2010. Geographic variation in dia- Laodelphax striatellus (Falleń) (Hemiptera: Delphacidae). Acta Entomol. pause induction: the grape berry moth (Lepidoptera: Tortricidae). Popul. Sinica. 51: 640–645 (in Chinese with English summary). Ecol. 39: 1751–1755. Zhang,H.Y.,Y.G.Diao,H.B.Yang,Y.Zhao,X.X.Zhang,andB.P. Umsalama, A.M.A., Z. H. Shi, Y. L. Guo, X. F. Zou, Z. P. Hao, and S. T. Zhai. 2011. Population dynamics and migration characteristics of the Pang. 2007. Maternal photoperiod effect on and geographic variation of small brown planthopper in spring in Jining, Shangdong Province. diapause incidence in Cotesia plutellae (Hymenoptera: Braconidae) from Chinese J. Appl. Entomol. 48: 1298–1308 (in Chinese with English China. Appl. Entomol. Zool. 42: 383–389. summary).